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. 1994 Apr 1;299(Pt 1):109–114. doi: 10.1042/bj2990109

Temporal regulation of the IgE-dependent 1,2-diacylglycerol production by tyrosine kinase activation in a rat (RBL 2H3) mast-cell line.

P Lin 1, S J Fung 1, S Li 1, T Chen 1, B Repetto 1, K S Huang 1, A M Gilfillan 1
PMCID: PMC1138028  PMID: 7513150

Abstract

We explored the possible role of tyrosine kinases in the IgE-dependent regulation of 1,2-diacylglycerol (DAG) production in RBL 2H3 cells. When triggered via their high-affinity IgE receptors (Fc epsilon RI), there was a rapid phosphorylation of tyrosine residues on a number of proteins. The phosphorylation of these proteins and ultimately histamine release were inhibited in a concentration-dependent manner by the tyrosine kinase inhibitor, tyrphostin. In cells labelled with [3H]myristic acid, we observed a characteristic biphasic increase in [3H]DAG production. In the presence of tyrosine kinase inhibitor, the initial increase in DAG was still observed, but the secondary increase, which was dependent on phosphatidylcholine-specific phospholipase D (PC-PLD) activation, was completely abolished. Tyrphostin significantly inhibited IgE-dependent activation of PC-PLD, suggesting that PC-PLD activation was regulated by tyrosine phosphorylation. Furthermore, when proteins from RBL 2H3 cells were immunoprecipitated with an anti-phosphotyrosine antibody, PC-PLD activity was recovered from the immunoprecipitated fraction. These results demonstrate that the secondary, but not the initial, phase of 1,2-DAG production in response to Fc epsilon RI aggregation is regulated by the initial activation of tyrosine kinases and that PC-PLD may be regulated directly by this mechanism.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anthes J. C., Eckel S., Siegel M. I., Egan R. W., Billah M. M. Phospholipase D in homogenates from HL-60 granulocytes: implications of calcium and G protein control. Biochem Biophys Res Commun. 1989 Aug 30;163(1):657–664. doi: 10.1016/0006-291x(89)92187-6. [DOI] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Beaven M. A., Cunha-Melo J. R. Membrane phosphoinositide-activated signals in mast cells and basophils. Prog Allergy. 1988;42:123–184. [PubMed] [Google Scholar]
  4. Beaven M. A., Rogers J., Moore J. P., Hesketh T. R., Smith G. A., Metcalfe J. C. The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J Biol Chem. 1984 Jun 10;259(11):7129–7136. [PubMed] [Google Scholar]
  5. Benhamou M., Gutkind J. S., Robbins K. C., Siraganian R. P. Tyrosine phosphorylation coupled to IgE receptor-mediated signal transduction and histamine release. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5327–5330. doi: 10.1073/pnas.87.14.5327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benhamou M., Siraganian R. P. Protein-tyrosine phosphorylation: an essential component of Fc epsilon RI signaling. Immunol Today. 1992 Jun;13(6):195–197. doi: 10.1016/0167-5699(92)90152-w. [DOI] [PubMed] [Google Scholar]
  7. Bourgoin S., Grinstein S. Peroxides of vanadate induce activation of phospholipase D in HL-60 cells. Role of tyrosine phosphorylation. J Biol Chem. 1992 Jun 15;267(17):11908–11916. [PubMed] [Google Scholar]
  8. Cunha-Melo J. R., Dean N. M., Moyer J. D., Maeyama K., Beaven M. A. The kinetics of phosphoinositide hydrolysis in rat basophilic leukemia (RBL-2H3) cells varies with the type of IgE receptor cross-linking agent used. J Biol Chem. 1987 Aug 25;262(24):11455–11463. [PubMed] [Google Scholar]
  9. Eiseman E., Bolen J. B. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature. 1992 Jan 2;355(6355):78–80. doi: 10.1038/355078a0. [DOI] [PubMed] [Google Scholar]
  10. Gruchalla R. S., Dinh T. T., Kennerly D. A. An indirect pathway of receptor-mediated 1,2-diacylglycerol formation in mast cells. I. IgE receptor-mediated activation of phospholipase D. J Immunol. 1990 Mar 15;144(6):2334–2342. [PubMed] [Google Scholar]
  11. Hutchcroft J. E., Harrison M. L., Geahlen R. L. B lymphocyte activation is accompanied by phosphorylation of a 72-kDa protein-tyrosine kinase. J Biol Chem. 1991 Aug 15;266(23):14846–14849. [PubMed] [Google Scholar]
  12. Inamori K., Sagawa N., Hasegawa M., Itoh H., Ueda H., Kobayashi F., Ihara Y., Mori T. Identification and partial characterization of phospholipase D in the human amniotic membrane. Biochem Biophys Res Commun. 1993 Mar 31;191(3):1270–1277. doi: 10.1006/bbrc.1993.1354. [DOI] [PubMed] [Google Scholar]
  13. Kawakami T., Inagaki N., Takei M., Fukamachi H., Coggeshall K. M., Ishizaka K., Ishizaka T. Tyrosine phosphorylation is required for mast cell activation by Fc epsilon RI cross-linking. J Immunol. 1992 Jun 1;148(11):3513–3519. [PubMed] [Google Scholar]
  14. Kennerly D. A. Diacylglycerol metabolism in mast cells. Analysis of lipid metabolic pathways using molecular species analysis of intermediates. J Biol Chem. 1987 Dec 5;262(34):16305–16313. [PubMed] [Google Scholar]
  15. Kennerly D. A., Sullivan T. J., Sylwester P., Parker C. W. Diacylglycerol metabolism in mast cells: a potential role in membrane fusion and arachidonic acid release. J Exp Med. 1979 Oct 1;150(4):1039–1044. doi: 10.1084/jem.150.4.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kumada T., Miyata H., Nozawa Y. Involvement of tyrosine phosphorylation in IgE receptor-mediated phospholipase D activation in rat basophilic leukemia (RBL-2H3) cells. Biochem Biophys Res Commun. 1993 Mar 31;191(3):1363–1368. doi: 10.1006/bbrc.1993.1367. [DOI] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Li W., Deanin G. G., Margolis B., Schlessinger J., Oliver J. M. Fc epsilon R1-mediated tyrosine phosphorylation of multiple proteins, including phospholipase C gamma 1 and the receptor beta gamma 2 complex, in RBL-2H3 rat basophilic leukemia cells. Mol Cell Biol. 1992 Jul;12(7):3176–3182. doi: 10.1128/mcb.12.7.3176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lin P. Y., Wiggan G. A., Gilfillan A. M. Activation of phospholipase D in a rat mast (RBL 2H3) cell line. A possible unifying mechanism for IgE-dependent degranulation and arachidonic acid metabolite release. J Immunol. 1991 Mar 1;146(5):1609–1616. [PubMed] [Google Scholar]
  20. Lin P., Fung W. J., Gilfillan A. M. Phosphatidylcholine-specific phospholipase D-derived 1,2-diacylglycerol does not initiate protein kinase C activation in the RBL 2H3 mast-cell line. Biochem J. 1992 Oct 1;287(Pt 1):325–331. doi: 10.1042/bj2870325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lin P., Gilfillan A. M. The role of calcium and protein kinase C in the IgE-dependent activation of phosphatidylcholine-specific phospholipase D in a rat mast (RBL 2H3) cell line. Eur J Biochem. 1992 Jul 1;207(1):163–168. doi: 10.1111/j.1432-1033.1992.tb17033.x. [DOI] [PubMed] [Google Scholar]
  22. Margolis B., Hu P., Katzav S., Li W., Oliver J. M., Ullrich A., Weiss A., Schlessinger J. Tyrosine phosphorylation of vav proto-oncogene product containing SH2 domain and transcription factor motifs. Nature. 1992 Mar 5;356(6364):71–74. doi: 10.1038/356071a0. [DOI] [PubMed] [Google Scholar]
  23. Martin T. W., Michaelis K. P2-purinergic agonists stimulate phosphodiesteratic cleavage of phosphatidylcholine in endothelial cells. Evidence for activation of phospholipase D. J Biol Chem. 1989 May 25;264(15):8847–8856. [PubMed] [Google Scholar]
  24. Nagao S., Nagata K., Kohmura Y., Ishizuka T., Nozawa Y. Redistribution of phospholipid/Ca2+-dependent protein kinase in mast cells activated by various agonists. Biochem Biophys Res Commun. 1987 Feb 13;142(3):645–653. doi: 10.1016/0006-291x(87)91463-x. [DOI] [PubMed] [Google Scholar]
  25. Park D. J., Min H. K., Rhee S. G. IgE-induced tyrosine phosphorylation of phospholipase C-gamma 1 in rat basophilic leukemia cells. J Biol Chem. 1991 Dec 25;266(36):24237–24240. [PubMed] [Google Scholar]
  26. Rando R. R. Regulation of protein kinase C activity by lipids. FASEB J. 1988 May;2(8):2348–2355. doi: 10.1096/fasebj.2.8.3282960. [DOI] [PubMed] [Google Scholar]
  27. Siraganian R. P. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal Biochem. 1974 Feb;57(2):383–394. doi: 10.1016/0003-2697(74)90093-1. [DOI] [PubMed] [Google Scholar]
  28. Song J. G., Pfeffer L. M., Foster D. A. v-Src increases diacylglycerol levels via a type D phospholipase-mediated hydrolysis of phosphatidylcholine. Mol Cell Biol. 1991 Oct;11(10):4903–4908. doi: 10.1128/mcb.11.10.4903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stanley J. B., Gorczynski R., Huang C. K., Love J., Mills G. B. Tyrosine phosphorylation is an obligatory event in IL-2 secretion. J Immunol. 1990 Oct 1;145(7):2189–2198. [PubMed] [Google Scholar]
  30. Stephan V., Benhamou M., Gutkind J. S., Robbins K. C., Siraganian R. P. Fc epsilon RI-induced protein tyrosine phosphorylation of pp72 in rat basophilic leukemia cells (RBL-2H3). Evidence for a novel signal transduction pathway unrelated to G protein activation and phosphatidylinositol hydrolysis. J Biol Chem. 1992 Mar 15;267(8):5434–5441. [PubMed] [Google Scholar]
  31. Uings I. J., Thompson N. T., Randall R. W., Spacey G. D., Bonser R. W., Hudson A. T., Garland L. G. Tyrosine phosphorylation is involved in receptor coupling to phospholipase D but not phospholipase C in the human neutrophil. Biochem J. 1992 Feb 1;281(Pt 3):597–600. doi: 10.1042/bj2810597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. WROBLEWSKI F., LADUE J. S. Lactic dehydrogenase activity in blood. Proc Soc Exp Biol Med. 1955 Oct;90(1):210–213. doi: 10.3181/00379727-90-21985. [DOI] [PubMed] [Google Scholar]
  33. Wang P., Anthes J. C., Siegel M. I., Egan R. W., Billah M. M. Existence of cytosolic phospholipase D. Identification and comparison with membrane-bound enzyme. J Biol Chem. 1991 Aug 15;266(23):14877–14880. [PubMed] [Google Scholar]
  34. White J. R., Pluznik D. H., Ishizaka K., Ishizaka T. Antigen-induced increase in protein kinase C activity in plasma membrane of mast cells. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8193–8197. doi: 10.1073/pnas.82.23.8193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yaish P., Gazit A., Gilon C., Levitzki A. Blocking of EGF-dependent cell proliferation by EGF receptor kinase inhibitors. Science. 1988 Nov 11;242(4880):933–935. doi: 10.1126/science.3263702. [DOI] [PubMed] [Google Scholar]
  36. Yu K. T., Lyall R., Jariwala N., Zilberstein A., Haimovich J. Antigen- and ionophore-induced signal transduction in rat basophilic leukemia cells involves protein tyrosine phosphorylation. J Biol Chem. 1991 Nov 25;266(33):22564–22568. [PubMed] [Google Scholar]

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